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Review Paper New Forests 6: 347-371,1992. 0 1992 Kluwer Academic Publishers. Printed in the Netherlands. Review paper Allozyme markers in forest genetic conservation C. I. MILLAR and R. D. WESTFALL Center for Conservation of Genetic Diversity, Institute of Forest Genetics, Pacific Southwest Forest and Range Experiment Station, USDA Forest Service, Box 245, Berkeley, CA 94701, USA Received 8 October 1990; accepted 2 April 1991 Key words: genetic diversity, isozymes, rare and endangered species, in-situ conservation, ex-situ conservation Application. Allozyme markers are useful in three main aspects of forest genetic conserva- tion: assessing the amount and distribution of genetic variation; determining sampling plans for in-situ and ex-situ conservation; and monitoring changes in genetic diversity. Since allozymes represent only one type of polymorphism, they are best used in conjunction with other traits when information about adaptive variation is needed. Abstract. Genetic diversity is important in tree-breeding, in managing rare and endangered tree species, and in maintaining healthy populations of widespread native tree species. Allozymes are useful in determining genetic relationships among species, where they can be used to assess affiliations of rare taxa and predict relative endangerment among species. Because allozymes sometimes yield different information about genetic variation within species than revealed by other traits, when estimates of total or adaptive genetic variation are important, allozymes are best used in conjunction with other traits. Allozymes are useful for measuring direct allelic diversity when designing ex-situ and in-situ conservation strate- gies. We demonstrate an application of canonical trend-surface analysis for determining locations of in-situ genetic conservation areas. Allozymes also serve as useful markers in monitoring the effects of forest management and other environmental changes on genetic diversity. Introduction Forest genetic conservation has its origins in the crop gene-resources movement (Frankel 1977). Initial concern focused primarily on economi- This article was written and prepared by U.S. Government employees on official time, and is therefore in the public domain. 348 tally important tree species, and on the importance of conserving germ- plasm for future benefits to tree breeding. Because commercial tree species, unlike agronomic crops, had long rotation times and were planted in wildland settings, diversity was important for adaptability as well as increased productivity. Within such a context, the goals and techniques of genetic conservation became interwoven with long-term tree-improvement strategies (e.g., FAO 1975; Kitzmiller 1976, 1990; Zobel 1977; Namkoong 1984). Increasing concern for environmental degradation has broadened the scope of genetic conservation to include non-commercial species, espe- cially rare or endangered taxa, for their intrinsic values (Namkoong 1986; Ledig 1986a, 1988a, b). Forest geneticists view as serious losses the species extinctions and systematic impoverishment of populations that are occurring not just in tropical ecosystems, but in temperate forests as well. Trees are also increasingly valued for their role in ecosystem functioning. As structurally large organisms, trees create the physical and biological habitats on which many other plants and animals depend for their survival. Allozymes in the service of genetic conservation For many of the same reasons that allozyme markers have been useful in other aspects of forest genetics, they find applications in a wide range of genetic conservation situations. Research and application in forest genetic conservation can be divided into three steps: Assessing, conserving, and monitoring genetic diversity. Genetic conservation borrows heavily from the cumulative research of forest genetics, using information about genetic architecture, mating systems, gene flow, etc. as input for many conserva- tion analyses. It is because so much basic knowledge exists about popula- tion genetic parameters in trees that we have been able to progress in conservation analyses beyond what has been possible in lesser known plants. Assessing genetic diversity Knowledge of baseline genetic diversity among and within species is needed for nearly all conservation analyses and applications. This infor- mation, whether measured or predicted, is essential for deciding what and how to conserve, for assessing whether genetic changes are occurring, and for determining whether genetic parameters are even relevant in a con- servation plan. Assessing baseline diversity goes beyond the inventory or 349 description of taxa and genetic variation. In most cases it includes an analysis of pattern in the data and attempts to interpret the pattern in light of evolutionary history and ecological context. Systematic studies Knowledge of species boundaries and genetic relationships among species are critical to conservation. Both by legal mandates and general consensus among conservation biologists, genetic resources of an individual species are usually given higher priority for protection against extinction than populations within a species. Although in the temperate zone species extinction in historical times has been infrequent in tree species, 233 woody plant species have been identified by the Center for Plant Con- servation as being of “significant conservation concern” in the United States (Falk 1990; Ledig 1991). For example, American chestnut (Castanea dentata) has been all but eliminated by an introduced blight early in this century (Burnham 1988). American elm (Ulmus americana) and white pines (Pinus sect. St&us) (Kinloch 1972) also have been devastated by introduced pathogens. The ranges of Port-Orford-cedar (Chamaecyparis lawsoniana) (Zobel et al. 1985) and Florida torreya (Torreya taxifoZia> (Godfrey and Kurz 1962) are being fragmented by diseases. Ozone and other pollutants are narrowing the gene pools of pines around urban areas, such as the Los Angeles basin (Miller 1973). Genetic diversity in Fraser fir (Abies fraseri) and red spruce (Picea rubens) in the Appalachains is being lost as a result of combined onslaughts by insects, climate change, heavy metal pollution and acid deposition (Hamburg and Cogbill 1988). In tropical forests, the rate of species extinction is high (Wilson 1988). Allozymes are useful for evaluating species boundaries because they provide more-or-less standard yardsticks that make comparisons among taxa meaningful (Strauss 1992, this issue, pp. 125-158). They are also less subject to problems of homoplasy (that is, similar traits occurring in distinct taxa that are not due to common ancestry) than traits traditionally used to evaluate taxonomy. Because endangered taxa at the species level are eligible for protection under endangered species legislation, taxonomic determinations carry legal implications. Although listing under plant pro- tection legislation involves an evaluation of many factors affecting endan- germent, one important consideration is the degree of genetic distinction of the taxon. Allozymes can provide a quantitative estimate of distinction, thereby helping to determine conservation priorities (Millar and Libby 1991). In some cases, allozymes may indicate that a taxon traditionally accepted as a rare species (and maybe already listed) is actually well within the range of variation of a more widespread species. In other cases, 350 allozymes may draw attention to distinct taxa that hadn’t been recognized on other grounds. Because of inconsistent correlations of allozyme with other traits (Hamrick and Godt 1989), conservation priorities probably should not be determined legalistically on allozymes alone, although they are important when combined with other data. The cypresses (Cupressus) of southwest United States and Baja Califor- nia provide an example. As many as 14 species (Wolf 1948) and as few as 7 (Little 1970) have been recognized, all of which occur as mosaics of disjunct populations associated with sterile soils. Santa Cruz cypress (C. abramsiuna) is federally and state-listed as endangered. We analyzed allozyme variation in 62 populations at 25 loci of all taxa in Baja Califor- nia and the United States, and found patterns of relationships that differed in some cases from those suggested by the published taxonomies.’ For example, there was no evidence that Santa Cruz cypress is a distinct taxon. Its five populations were well within the range of variation of the Sargent cypress (C. surge&i) complex. The Santa Cruz cypress populations had lower genetic distance to populations of other taxa than to each other. The five populations of Tecate cypress (C. forbesii) in California, which were petitioned for state listing, were also within the range of another taxon, the Arizona cypress complex (C. arizonicu, C. glubru). A sixth population of Tecate cypress, however, on Guadalupe Island, Mexico, was distinct from this group. Cuyamaca cypress (C. stephensonii), known from one small and declining population in the United States, but not currently being considered for listing, was a distinct taxon allozymically. In almost all taxa, the populations with the smallest sizes were more divergent. In another example, Prober et al. (1990a) analyzed allozyme variation of the 12 “green ash” species of Eucalyptus, which include several rare species of conservation interest, and identified several relationships that had been either poorly resolved or intractable to morphological analysis. A major difference
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